Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment
As with many physiological performance traits, the capacity of endotherms to thermoregulate declines with age. Aging compromises both the capacity to conserve or dissipate heat and the thermogenesis, which is fueled by aerobic metabolism. The rate of metabolism, however, not only determines thermoge...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-11-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2020.576304/full |
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| author | Marta Grosiak Paweł Koteja Ulf Bauchinger Ulf Bauchinger Edyta T. Sadowska |
| author_facet | Marta Grosiak Paweł Koteja Ulf Bauchinger Ulf Bauchinger Edyta T. Sadowska |
| author_sort | Marta Grosiak |
| collection | DOAJ |
| description | As with many physiological performance traits, the capacity of endotherms to thermoregulate declines with age. Aging compromises both the capacity to conserve or dissipate heat and the thermogenesis, which is fueled by aerobic metabolism. The rate of metabolism, however, not only determines thermogenic capacity but can also affect the process of aging. Therefore, we hypothesized that selection for an increased aerobic exercise metabolism, which has presumably been a crucial factor in the evolution of endothermic physiology in the mammalian and avian lineages, affects not only the thermoregulatory traits but also the age-related changes of these traits. Here, we test this hypothesis on bank voles (Myodes glareolus) from an experimental evolution model system: four lines selected for high swim-induced aerobic metabolism (A lines), which have also increased the basal, average daily, and maximum cold-induced metabolic rates, and four unselected control (C) lines. We measured the resting metabolic rate (RMR), evaporative water loss (EWL), and body temperature in 72 young adult (4 months) and 65 old (22 months) voles at seven ambient temperatures (13–32°C). The RMR was 6% higher in the A than in the C lines, but, regardless of the selection group or temperature, it did not change with age. However, EWL was 12% higher in the old voles. An increased EWL/RMR ratio implies either a compromised efficiency of oxygen extraction in the lungs or increased skin permeability. This effect was more profound in the A lines, which may indicate their increased vulnerability to aging. Body temperature did not differ between the selection and age groups below 32°C, but at 32°C it was markedly higher in the old A-line voles than in those from other groups. As expected, the thermogenic capacity, measured as the maximum cold-induced oxygen consumption, was decreased by about 13% in the old voles from both selection groups, but the performance of old A-line voles was the same as that of the young C-line ones. Thus, the selection for high aerobic exercise metabolism attenuated the adverse effects of aging on cold tolerance, but this advantage has been traded off by a compromised coping with hot conditions by aged voles. |
| first_indexed | 2024-12-11T04:15:33Z |
| format | Article |
| id | doaj.art-881d1e692330462191dfea669a1856ba |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-11T04:15:33Z |
| publishDate | 2020-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-881d1e692330462191dfea669a1856ba2022-12-22T01:21:15ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-11-011110.3389/fphys.2020.576304576304Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection ExperimentMarta Grosiak0Paweł Koteja1Ulf Bauchinger2Ulf Bauchinger3Edyta T. Sadowska4Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, PolandInstitute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, PolandInstitute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, PolandNencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw, PolandInstitute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, PolandAs with many physiological performance traits, the capacity of endotherms to thermoregulate declines with age. Aging compromises both the capacity to conserve or dissipate heat and the thermogenesis, which is fueled by aerobic metabolism. The rate of metabolism, however, not only determines thermogenic capacity but can also affect the process of aging. Therefore, we hypothesized that selection for an increased aerobic exercise metabolism, which has presumably been a crucial factor in the evolution of endothermic physiology in the mammalian and avian lineages, affects not only the thermoregulatory traits but also the age-related changes of these traits. Here, we test this hypothesis on bank voles (Myodes glareolus) from an experimental evolution model system: four lines selected for high swim-induced aerobic metabolism (A lines), which have also increased the basal, average daily, and maximum cold-induced metabolic rates, and four unselected control (C) lines. We measured the resting metabolic rate (RMR), evaporative water loss (EWL), and body temperature in 72 young adult (4 months) and 65 old (22 months) voles at seven ambient temperatures (13–32°C). The RMR was 6% higher in the A than in the C lines, but, regardless of the selection group or temperature, it did not change with age. However, EWL was 12% higher in the old voles. An increased EWL/RMR ratio implies either a compromised efficiency of oxygen extraction in the lungs or increased skin permeability. This effect was more profound in the A lines, which may indicate their increased vulnerability to aging. Body temperature did not differ between the selection and age groups below 32°C, but at 32°C it was markedly higher in the old A-line voles than in those from other groups. As expected, the thermogenic capacity, measured as the maximum cold-induced oxygen consumption, was decreased by about 13% in the old voles from both selection groups, but the performance of old A-line voles was the same as that of the young C-line ones. Thus, the selection for high aerobic exercise metabolism attenuated the adverse effects of aging on cold tolerance, but this advantage has been traded off by a compromised coping with hot conditions by aged voles.https://www.frontiersin.org/articles/10.3389/fphys.2020.576304/fullagingbank volebody temperatureevolutionmetabolic ratethermal conductance |
| spellingShingle | Marta Grosiak Paweł Koteja Ulf Bauchinger Ulf Bauchinger Edyta T. Sadowska Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment Frontiers in Physiology aging bank vole body temperature evolution metabolic rate thermal conductance |
| title | Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment |
| title_full | Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment |
| title_fullStr | Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment |
| title_full_unstemmed | Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment |
| title_short | Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment |
| title_sort | age related changes in the thermoregulatory properties in bank voles from a selection experiment |
| topic | aging bank vole body temperature evolution metabolic rate thermal conductance |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2020.576304/full |
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